The Top 10 oomycete pathogens in molecular plant pathology

Review

The Top 10 oomycete pathogens in molecular plant pathology

SOPHIEN KAMOUN1,*, OLIVER FURZER1, JONATHAN D. G. JONES1, HOWARD S. JUDELSON2,GUL SHAD ALI3, RONALDO J. D. DALIO4, SANJOY GUHA ROY5, LEONARDO SCHENA6,ANTONIOS ZAMBOUNIS7, FRANCK PANABIÈRES8, DAVID CAHILL9, MICHELINA RUOCCO10,ANDREIA FIGUEIREDO11, XIAO-REN CHEN12, JON HULVEY13, REMCO STAM14, KURT LAMOUR15,MARK GIJZEN16, BRETT M. TYLER17, NIKLAUS J. GRÜNWALD18, M. SHAHID MUKHTAR19,20,DANIEL F. A. TOMÉ21, MAHMUT TÖR22, GUIDO VAN DEN ACKERVEKEN23, JOHN MCDOWELL24,FOUAD DAAYF25, WILL IAM E. FRY26, HANNELE LINDQVIST-KREUZE27, HAROLD J. G. MEIJER28,BENJAMIN PETRE1,29, JEAN RISTAINO30, KENTARO YOSHIDA1, PAUL R. J. B IRCH14 ANDFRANCINE GOVERS28

1The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, UK2Department of Plant Pathology and Microbiology, University of California, Riverside, CA 92521, USA3Department of Plant Pathology and MREC, IFAS, University of Florida, Apopka, FL 32703, USA4Biotechnology Laboratory, Centro de Citricultura Sylvio Moreira/Instituto Agronomico, Cordeirópolis-Sao Paulo 13490-970, Brazil5Department of Botany, West Bengal State University, Barasat, Kolkata-700126, India6Dipartimento di Gestione dei Sistemi Agrari e Forestali, Università degli Studi Mediterranea, 89122 Reggio Calabria, Italy7UMR1290 BIOGER-CPP, INRA-AgroParisTech, 78850 Thiverval-Grignon, France8INRA, UMR1355, Université Nice Sophia Antipolis, CNRS, UMR7254, ISA, F-06903 Sophia Antipolis, France9Deakin University, Geelong, Vic. 3217, Australia10Portici Division of the Italian National Research Council (CNR), Institute for Sustainable Plant Protection (IPSP), Via Università 133, 80055 Portici (NA), Italy11Centre for Biodiversity, Functional and Integrative Genomics, Faculty of Sciences, University of Lisboa, 1749-016 Lisbon, Portugal12College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, 225009, China13Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA 01003, USA14Division of Plant Sciences, College of Life Sciences, University of Dundee (at James Hutton Institute), Errol Road, Invergowrie, DD2 5DA, UK15Department of Entomology and Plant Pathology, University of Tennessee, TN 37996, USA16Agriculture and Agri-Food Canada, 1391 Sandford Street, London, ON, Canada, N5V 4T317Center for Genome Research and Biocomputing and Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA18USDA ARS, Plant Pathology Horticultural Crops Research Lab. 3420 NW Orchard Ave., Corvallis, Oregon 97330, United States19Department of Biology, University of Alabama at Birmingham, Birmingham, AL 35294-1170, USA20Nutrition Obesity Research Center, University of Alabama at Birmingham, Birmingham, AL 35294, USA21School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK22National Pollen and Aerobiology Research Unit, The University of Worcester, Henwick Grove, Worcester, WR2 6AJ, UK23Plant–Microbe Interactions, Department of Biology, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands24Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, Blacksburg, VA 24061, USA25Department of Plant Science, University of Manitoba, Winnipeg, MB R3T 2N2, Canada26Department of Plant Pathology and Plant–Microbe Biology, Cornell University, Ithaca, NY 14853, USA27International Potato Center, Apartado 1558, Lima 12, Peru28Laboratory of Phytopathology, Wageningen University, NL-1-6708 PB Wageningen, the Netherlands29INRA, UMR1136 Interactions Arbres/Microorganismes, Centre INRA Nancy Lorraine, 54280 Champenoux, France30Department of Plant Pathology, North Carolina State University, Raleigh, NC 27695, USA

SUMMARY

Oomycetes form a deep lineage of eukaryotic organisms thatincludes a large number of plant pathogens which threatennatural and managed ecosystems.We undertook a survey to querythe community for their ranking of plant-pathogenic oomycete

species based on scientific and economic importance. In total, wereceived 263 votes from 62 scientists in 15 countries for a totalof 33 species. The Top 10 species and their ranking are: (1)Phytophthora infestans; (2, tied) Hyaloperonospora arabidopsidis;(2, tied) Phytophthora ramorum; (4) Phytophthora sojae; (5)Phytophthora capsici; (6) Plasmopara viticola; (7) Phytophthoracinnamomi; (8, tied) Phytophthora parasitica; (8, tied) Pythiumultimum; and (10) Albugo candida. This article provides an*Correspondence: Email: [email protected]

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MOLECULAR PLANT PATHOLOGY (2015) 16 (4) , 413–434 DOI: 10.1111/mpp.12190

© 2014 BSPP AND JOHN WILEY & SONS LTD 413

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introduction to these 10 taxa and a snapshot of current research.We hope that the list will serve as a benchmark for future trendsin oomycete research.

Keywords: oomycetes plant pathology, microbiology, diversity,genomics.

INTRODUCTION

Oomycetes are eukaryotic organisms that superficially resemblefilamentous fungi, but are phylogenetically related to diatoms andbrown algae in the stramenopiles (Gunderson et al., 1987; Jiangand Tyler, 2012; Lamour and Kamoun, 2009; Thines, 2014; Thinesand Kamoun, 2010). Fossil evidence indicates that a number ofoomycetes emerged as endophytes of land plants at least by theCarboniferous period, approximately 300–350 million years ago(Krings et al., 2011). One species, Combresomyces williamsonii,described from ∼320-million-year-old petrified stem cortex androotlets of a seed fern, may have even been parasitic(Strullu-Derrien et al., 2011). Phylogenetic analyses of modern taxahave revealed that plant parasitism has evolved independently inthree lineages of oomycetes (Thines and Kamoun, 2010).Well-known plant pathogens, namely downy mildews,Phytophthora and Pythium, appear to have radiated from acommon plant-parasitic ancestor (Thines and Kamoun, 2010). Theimpact of oomycetes on humankind is well documented as both apersistent threat to subsistence and commercial farming and asdestructive pathogens of native plants (Agrios, 2005; Erwin andRibeiro, 1996;Lamour and Kamoun, 2009).As a result,news relatedto plant diseases caused by oomycetes tends to capture the interestof the general public and is frequently featured in the media.

In the last two decades, increased awareness of the distinctivephylogeny and biology of oomycetes has driven the emergence ofa specialist research community that is currently organized under

the umbrella of the ‘Oomycete Molecular Genetics Network’. Thiscommunity has moved the field beyond the gloomy view of the1980s that oomycetes are a ‘fungal geneticist’s nightmare’ (Shaw,1983; discussed in Schornack et al., 2009). It has produced novelparadigms in understanding host–microbe interactions, effectorbiology and genome evolution (Bozkurt et al., 2012; Govers andGijzen, 2006; Jiang and Tyler, 2012; Schornack et al., 2009;Vleeshouwers et al., 2011). The oomycete community was one ofthe first in plant pathology to initiate coordinated transcriptomeand genome sequencing projects, and subsequently to exploit theresulting resources to drive conceptual advances (Govers andGijzen, 2006; Pais et al., 2013; Schornack et al., 2009). These days,with the genomes serving as unique resources for basic andapplied research, oomycetes are best portrayed as a ‘genomicist’sdream’ (Govers and Gijzen, 2006; Jiang and Tyler, 2012; Pais et al.,2013; Schornack et al., 2009).

It is therefore particularly fitting that the oomycetes are at lastcovered by the Top 10 review series of Molecular Plant Pathology.The process to generate the list and the aim of this article aresimilar to those of previous contributions on plant-pathogenicviruses (Scholthof et al., 2011), fungi (Dean et al., 2012), bacteria(Mansfield et al., 2012) and nematodes (Jones et al., 2013). Weundertook a survey to query the community for their ranking ofplant-pathogenic oomycete taxa based on scientific and economicimportance. In total, we received 263 votes from 62 scientists in 15countries that yielded the Top 10 species (Table 1). To somedegree, the results reflect the sizes of the subcommunities. Six ofthe ten species belong to the genus Phytophthora, which ismore commonly studied than any other oomycete genus.Obligate parasites are also well represented with three species(Hyaloperonospora arabidopsidis, Plasmopara viticola and Albugocandida, Table 1). Another 23 species received votes but rankedoutside the Top 10 (Table 2). The fish parasite Saprolegniaparasitica received enough votes to place it in the Top 10, butwas removed, given that the list focuses on plant pathogens(Table 2).

Table 1 Top 10 oomycetes in molecular plant pathology.

Rank Species Common disease name(s)Number of papers(2005–2014)

Number ofvotes

1 Phytophthora infestans Late blight 1230 51= 2 Hyaloperonospora arabidopsidis Downy mildew 137 25= 2 Phytophthora ramorum Sudden oak death; Ramorum disease 378 254 Phytophthora sojae Stem and root rot 276 225 Phytophthora capsici Blight; stem and fruit rot; various others 541 176 Plasmopara viticola Downy mildew 326 157 Phytophthora cinnamomi Root rot; dieback 315 13= 8 Phytophthora parasitica Root and stem rot; various others 142 10= 8 Pythium ultimum Damping off; root rot 319 1010 Albugo candida White rust 65 9

The ‘=’ sign before the ranking indicates that the species tied for that position. The number of papers published in 2005–2014 is based on searches of the Scopusdatabase (http://www.scopus.com) using the species names as a query. For H. arabidopsidis, a search for the alternative name ‘Peronospora parasitica’ was alsoperformed and the combined number is shown. Searches with the terms ‘oomycete*’ and ‘Phytophthora’ yielded 2068 and 4059 articles, respectively.

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This article is based on contributions from the voters to providean introduction to the 10 taxa and a snapshot of current research.Each section starts with a brief overview of the selected species,e.g. its importance, pathology, host range and life cycle. This isfollowed by a review of current research themes, particularly theunique findings that have emerged from the study of particularspecies, and an outlook on future research. We hope that thisarticle will serve as a reference and resource for novice and experi-enced readers alike, as well as provide a benchmark for futuretrends in oomycete research.

1. PHYTOPHTHORA INFESTANS

Phytophthora infestans causes potato late blight (Fig. 1), a disease withmajor historical impact. Providing twice the calories of rye and wheat perhectare, potato was central to European agriculture between 1750 and 1850.In 1844, the arrival of P. infestans changed this situation. In addition to thewell-documented Irish famine (Fig. 2), crop failures in 1845 and 1846 con-tributed to an estimated 750 000 hunger-associated deaths in continentalEurope (Zadoks, 2008). The discovery that late blight was caused by amicrobial pathogen, 15 years before Pasteur’s formal confirmation of GermTheory, places the 19th century migration of P. infestans as a significantmilestone in the foundation of plant pathology as a scientific discipline.Today, late blight remains a major constraint to the production of potato, theworld’s third largest staple crop, and is thus a constant threat to foodsecurity (Fisher et al., 2012; Haverkort et al., 2008).

In the 1840s, trade in potatoes probably facilitated the long-distancemigration of the pathogen. Whole-genome sequencing of European her-barium samples has revealed that populations belonging to the HERB-1genotype were different from US-1, the genotype dominating the populationglobally in the mid- to late 20th century (Goodwin et al., 1994; Martin et al.,2013, 2014; Yoshida et al., 2013, 2014). Waves of migration and genotypedisplacements in the 20th century have been well documented. The intro-duction of the A2 mating type to Europe in the 1970s (Drenth et al., 1994)

and, more recently, the emergence of new, more aggressive lineages, such as13_A2 (Blue 13) in Europe (Cooke et al., 2012), US-22 in the eastern USA (Fryet al., 2013; Hu et al., 2012) and US-23/US-24 in Canada (Peters et al.,2014), impose constant challenges to disease resistance breeding.

In the 1990s, P. infestans research led to the development of molecularapproaches to study oomycete pathology and biology. The first DNA trans-formation system (Judelson et al., 1991) and the first transcriptional profilingduring infection (Pieterse et al., 1991) paved the way to detailed molecularinvestigations of sexual and asexual development and pathogenicity(reviewed in Judelson, 1997). DNA fingerprinting revolutionized populationstudies (Goodwin et al., 1992) and was a prelude to the first genome-widegenetic map of a Phytophthora species (van der Lee et al., 1997). Observa-tions that gene silencing occurred in P. infestans transformants (e.g.Judelson and Whittaker, 1995) sparked important studies of the mechanismsunderlying transcriptional silencing (van West et al., 1999). The first large-scale transcript sequencing studies (Kamoun et al., 1999) ushered in thegenomics era of Phytophthora research.

Table 2 Other oomycete species that received votes.

Rank Species

11 Aphanomyces euteiches12 Albugo laibachii13 Bremia lactucae14 Phytophthora palmivora15 Pseudoperonospora cubensis16 Plasmopara halstedii17 Peronophythora litchi18 Peronosclerospora sorghi19 Peronospora belbahrii20 Phytophthora alni21 Phytophthora brassicae22 Phytophthora cactorum23 Phytophthora meadii24 Phytophthora phaseoli25 Phytophthora plurivora (formerly P. citricola)26 Plasmopara obducens27 Pythium aphanidermatum28 Pythium oligandrum29 Sclerophthora rayssiae30 Hyaloperonospora brassicaeNR Saprolegnia parasitica (fish parasite)NR Lagenidium giganteum (mosquito parasite)NR Pythium insidiosum (mammalian parasite)

NR, not ranked because the species is not associated with plants.

Fig. 1 Potato plants with typical late blight lesions. Infection starts when aspore lands on the leaf and germinates. The germ tube forms anappressorium and an emerging penetration peg pushes into an epidermalcell. Then the inner cell layers are colonized. During the biotrophic phase,hyphae grow in the intercellular space, whereas haustoria enter plant cellcavities and invaginate host cell plasma membrane. Later, Phytophthorainfestans switches to necrotrophic growth, resulting in the death of plantcells and the appearance of necrotic lesions on the infected tissues. In thisphase, hyphae escape through the stomata and produce numerous asexualspores, named sporangia, that easily detach and disperse by wind or water. Asporangium that finds a new host can either germinate directly and initiate anew cycle or, at lower temperatures, undergo cleavage resulting in azoosporangium from which six to eight flagellated spores are released. Thesezoospores can swim for several hours but, once they touch a solid surface,they encyst and germinate to initiate new infections. Under favourableconditions, the pathogen can complete the cycle from infection to sporulationin 4 days. In the field, this cycle is repeated multiple times during onegrowing season, resulting in billions of spores and a continuous increase indisease pressure. In addition to leaves, stems and tubers are also infectedand P. infestans can continue to flourish on the decaying plant material. Ifnot managed properly, infected seed potatoes or waste on refuse piles areoften the sources of inoculum for new infections in the spring. An alternativeroute for surviving the winter is via oospores, sexual spores that can survivein the soil for many years. Phytophthora infestans is heterothallic; isolates areeither A1 or A2 mating type, and sex organs only develop when isolates ofopposite mating type sense the sex hormone produced by the mate.

Top 10 oomycete plant pathogens 415

© 2014 BSPP AND JOHN WILEY & SONS LTD MOLECULAR PLANT PATHOLOGY (2015) 16(4 ) , 413–434

In the last 15 years, advanced genomic and functional approaches haveplaced P. infestans at the forefront of research to understand oomycetedevelopment (Judelson and Blanco, 2005) and pathogenicity (Kamoun,2006). An elegant combination of bioinformatics, proteomics and functionalgenomics has revealed secreted proteins as potential factors influencinghost–P. infestans interactions (Torto et al., 2003). Apoplastic effectors thatinhibit host secreted proteases were first described in P. infestans (Tianet al., 2004), and the apoplastic phytotoxin-like SCR74 (Liu et al., 2005)provided support for the use of diversifying selection as a criterion for theidentification of candidate effectors. The apoplastic effectors EPIC1 andEPIC2B were found to converge on the host protease RCR3, which is alsotargeted by an independently evolved effector from a fungal plant pathogen(Song et al., 2009). Recently, diversifying selection of the EPIC1 proteaseinhibitor was implicated in functional adaptation to the equivalent proteasetarget after ‘jumps’ to a new host (Dong et al., 2014).

The first reported P. infestans avirulence effector was AVR3a, the counter-part of resistance protein R3a (Armstrong et al., 2005). Comparison withavirulence effectors from Phytophthora sojae and H. arabidopsidis identifiedconserved amino acid motifs RXLR and EER (Rehmany et al., 2005), whichact as signals for translocation into host cells (Whisson et al., 2007). Thegenome sequence of P. infestans revealed hundreds of genes predicted toencode RXLR effectors, plus a second class of candidate effectors calledCrinklers (CRNs) (Haas et al., 2009), which may also be delivered inside plantcells (Schornack et al., 2010). These effector genes are rapidly evolving andare typically variable between different P. infestans isolates (Cooke et al.,2012). RXLR and CRN reside in gene-sparse, repeat-rich regions, potentiallysubject to rearrangement and rapid mutation, raising the concept of a‘two-speed’ genome in evolutionary terms (Haas et al., 2009; Raffaele et al.,2010). Recent years have witnessed intense efforts to determine the bio-chemical function of RXLR effectors, notably by determining their proteintargets in the host. The first target identified was ubiquitin E3 ligase CMPG1,

which AVR3a stabilizes to prevent programmed cell death in response toelicitors such as INF1 (Bos et al., 2010).

Breeding for late blight resistance was initiated by James Torbitt of Belfastin the 1870s, inspired by the theories of Charles Darwin, with whom heshared considerable correspondence (DeArce, 2008). More than 130 yearslater, breeding efforts have yet to provide a durable solution. Occasionally,local successes are reported; for example, variety C88, widely cultivated inChina for over a decade, retains its resistance (Li et al., 2011). Many resist-ance (R) genes effective against races of P. infestans have been identified(Rodewald and Trognitz, 2013). Only with the recent identification ofavirulence genes, all of which encode RXLR effectors, can breeders incorpo-rate knowledge on how P. infestans evades detection into their breedingstrategies (Vleeshouwers et al., 2011). Such information is critical for theprediction of the durability of R genes. The use of effectors as tools to rapidlyidentify R genes is a powerful step towards rational selection and combina-tion of lasting resistance (Vleeshouwers et al., 2008).

We still know relatively little about how P. infestans effectors manipulatehost plants to establish disease. How do they translocate into host cells? Dothey define host range? How do they work in concert to modulate complexnetworks of regulatory processes occurring in the host? Only recentlyhave researchers started to adopt structural biology to fully investigatefunctional relationships between interacting pathogen and plant proteins(Wirthmueller et al., 2013). Could such research catalyse the modification ofmolecular interactions in favour of the plant immune system through syn-thetic biology approaches?

The basic knowledge gained on P. infestans in the last decade is startingto have an impact on the management of late blight disease. For the controlof late blight, farmers largely rely on agrochemicals, many with unknownmodes of action. The emergence of insensitive strains is possibly a result ofhigh mutation rates in the pathogen (Randall et al., 2014). The phenylamidemetalaxyl was one of the first chemicals to exhibit specificity to oomycetes.Soon after its introduction and widespread use, fully insensitive strainsemerged, but only 35 years later was the molecular basis of this insensitivityuncovered (Randall et al., 2014). Mining of the P. infestans genome hasrevealed many novel proteins with domain combinations that are unique tooomycetes (Seidl et al., 2011). Several probably function in signalling andmay be promising fungicide targets. Mode-of-action studies are more acces-sible thanks to the available genomics resources, transformation tools andmarker strains with tags to visualize the cytoskeleton and various subcellularcompartments (Ah Fong and Judelson, 2003; Meijer et al., 2014). In resist-ance breeding, the efficacy of stacking R genes into favoured cultivars, byeither introgression or trans- or cis-genesis, is being investigated (Tan et al.,2010). However, for success, the R genes to be combined should be selectedcarefully on the basis of our knowledge on the variation in the pathogenpopulation, and the attendant vulnerability to resistance being overcome(Vleeshouwers et al., 2011). Future efforts should consider the introductionof multiple barriers, perhaps combining R proteins with, for instance,membrane-localized pattern recognition receptors or components governingnon-host resistance to P. infestans. Even then, it is unlikely that plant resist-ance can fully control late blight. Agrochemicals should not be abandoned.On the contrary, for more rational fungicide design, novel targets should beidentified, an endeavour that will be enhanced by an even more profoundinsight into the biology of P. infestans.

Fig. 2 One of the many Great Famine memorials around the world. Thesesculptures on Customs House Quays in Dublin, by artist Rowan Gillespie,stand as if walking towards the emigration ships on the Dublin Quayside(courtesy of Michael Seidl).



2. HYALOPERONOSPORA ARABIDOPSIDIS

Hyaloperonospora arabidopsidis (formerly H. parasitica and Peronosporaparasitica) is one of 700 downy mildew species within the Peronosporaceae(Thines, 2014). Downy mildew pathogens cause harmful diseases on manyimportant crops, notably Peronospora and Hyaloperonospora spp. onbrassica crops, Plasmopara viticola on grape, Peronosclerospora spp. onmaize and sorghum, Pseudoperonospora cubensis on cucurbits and Bremialactucae on lettuce (Lucas et al., 1995).

Most downy mildews have narrow host ranges and are completelydependent on their host for growth and reproduction.They can survive in thesoil as quiescent oospores that initiate infection through roots. Spread of thepathogen mostly occurs through airborne sporangiospores that are formedon the lower leaf surface, giving downy patches (Fig. 3). These spores ger-minate on the plant surface and penetrate by forming appressoria (Kochand Slusarenko, 1990). Once past the epidermis, hyphae grow intercellularlyand, similar to Phytophthora spp. and other downy mildews, develophaustoria, specialized structures that may function in feeding and the sup-pression of host defence by targeted secretion of effectors (Fig. 4, Whissonet al., 2007).

Hyaloperonospora arabidopsidis is a prominent pathogen in natural popu-lations of Arabidopsis thaliana (Coates and Beynon, 2010; Holub, 2008). Assuch, it was adopted in the 1980s as one of two pathogens of Arabidopsis,together with the bacterium Pseudomonas syringae (Koch and Slusarenko,1990).The Top 10 ranking of H. arabidopsidis reflects the subsequent successof the Arabidopsis–H. arabidopsidis pathosystem. H. arabidopsidis was ini-tially utilized as a ‘physiological probe’ of the Arabidopsis immune system(Holub et al., 1994). This research led to the cloning of the first plant diseaseR genes against an oomycete, better understanding of the evolutionarydynamics of R genes, the definition of broadly important immune systemregulators, the identification of downy mildew-resistant mutants and geneticdefinition of the complexity of the plant immune signalling network(reviewed in Coates and Beynon, 2010; Lapin and Van den Ackerveken, 2013;Slusarenko and Schlaich, 2003). On the pathogen side, research is hamperedby the lack of protocols for culture and genetic transformation, establishedtechniques with other oomycetes such as P. infestans. However, work in theearly 2000s led to the development of genetic maps and DNA libraries thatenabled the discovery of the first avirulence effector (Allen et al., 2004), andlater to the RXLR effector family (Rehmany et al., 2005).

Genome sequencing of H. arabidopsidis isolate Emoy2, completed in2010, unveiled 134 predicted RXLR effectors and other components of theH. arabidopsidis secretome (Baxter et al., 2010). Notably, this report alsorevealed important genomic signatures of obligate biotrophy that haveevolved convergently in other obligate oomycete and fungal lineages(reviewed in McDowell, 2011). Protein interaction assays have shown thatH. arabidopsidis effectors target a highly interconnected host machinery,helping to define a representative plant–pathogen interaction network(Mukhtar et al., 2011). In addition, several high-throughput functionalstudies have investigated effector subcellular localizations, suppression ofimmune responses, molecular targets and cognate immune receptors (Cabralet al., 2011, 2012; Caillaud et al., 2011; Fabro et al., 2011).

Future studies with the H. arabidopsidis experimental system will include:(i) direct or Agrobacterium-mediated transformation for genetic manipula-tion required for the molecular analysis of downy mildew pathogenicity; (ii)the establishment of the temporal hierarchy of effectors during penetration,colonization and sporulation, which may serve as a blueprint for a betterunderstanding of the molecular basis of biotrophy; (iii) the role of geneticrecombination and epigenetics on the emergence of new effectors; (iv) thedevelopment of tools to understand how plant-originated molecules regu-late pathogen response; and (v) the relevance of interspecies transfer ofsmall RNAs.These investigations on H. arabidopsidis will continue to providenew insights into the molecular mechanisms of downy mildew pathogenic-ity, and contribute to comparative and functional analysis of (obligate)biotrophic oomycete and fungal pathogens.

Fig. 3 Hyaloperonospora arabidopsidis disease symptoms on a 2-week-oldArabidopsis seedling. Mature sporangiophores are visible as white structureson the right side of the leaf.

Fig. 4 Diagram depicting a compatible interaction betweenHyaloperonospora arabidopsidis and Arabidopsis initiated by asporangiospore landing on the leaf surface. A, appressorium; C, cuticle; Ha,haustorium; Hy, hyphae; LE, lower epidermis; N, nucleus; PM, palisademesophyll cells; S, sporangiospore; SM, spongy mesophyll cells; Sp, maturesporangiophore; UE, upper epidermis. Note: sporangiophores are not drawnto scale.



3. PHYTOPHTHORA RAMORUM

Phytophthora ramorum is the most destructive disease of oaks worldwideand the cause of sudden oak death, sudden larch death and ramorum blight(Brasier and Webber, 2010; Grünwald et al., 2008; Rizzo et al., 2005; Werreset al., 2001) (Fig. 5).The host range of P. ramorum is one of the widest of anyPhytophthora spp., and includes many species of hardwood trees and orna-mentals. To date, four distinct clonal lineages have been recognized byvarious molecular markers and two mating types have been found(Grünwald et al., 2009; Van Poucke et al., 2012). These lineages appear to beanciently diverged, yet have emerged repeatedly in both North America andEurope (Goss et al., 2009a; Grünwald et al., 2012) (Fig. 6). Lineages NA1,NA2 and EU1 are currently found in Canada and the USA, whereas EU1 andEU2 exist in Europe (Goss et al., 2009b, 2011; Grünwald et al., 2012; VanPoucke et al., 2012). These lineages differ in aggressiveness in controlledassays, but field experiments have not been conducted given quarantinerestrictions (Elliott et al., 2011; Grünwald et al., 2008; Hüberli et al., 2012;Kasuga et al., 2012; Van Poucke et al., 2012). Unique ecological attributes,such as a wide host range and survival in dry, hot Mediterranean summers,combined with the ability to reproduce from chlamydospores, are thought toprovide the basis for sudden oak death in California (Garbelotto and Hayden,2012).

The availability of the genome sequence just a few years after the iden-tification of the pathogen provided rapid and novel insights into the biologyof this pathogen (Tyler et al., 2006). Like other Phytophthora spp.,P. ramorum has a large number of candidate effectors interacting with theplant hosts, including RXLR, CRNs and the necrosis and ethylene-inducingpeptide 1 (Nep1)-like protein (NLP) gene families (Goss et al., 2013; Tyleret al., 2006). RXLR effectors diversify rapidly, despite the clonality of thisorganism, using mechanisms such as loss or gain of repeated domains,recombination or gene conversion among paralogues and selection on pointmutations (Goss et al., 2013). Recent work has focused on the discovery ofendogenous small RNAs and description of the silencing machinery(Fahlgren et al., 2013). Phytophthora ramorum and two other Phytophthoraspp. examined produce two primary, distinct 21- and 25-nucleotide smallRNA classes, including a novel microRNA family. Two argonaute classes andtwo dicer-like proteins appear to be involved in each pathway (Fig. 7), butthis remains to be formally tested. Epigenetic mechanisms have been impli-cated recently in phenotypic diversification, namely colony morphology,colony senescence and virulence on coast live oak and California bay laurel(Kasuga et al., 2012).

Phytophthora ramorum provides a unique opportunity for the study of theevolution of a genome that has two mating types, yet appears to lack sexualreproduction in the known field populations. The epigenome, transcriptomeand proteome of P. ramorum remain a mystery. The apparent documentedphenotypic variation driven by host association might be epigenetic innature and invites further study. Several basic questions remain unanswered.Why does P. ramorum have such a large number of RXLR effectors,given that the genome is adapted to a wide host range? What are the genesconferring a wide host range compared with P. infestans and P. sojae? Isthere a centre of origin? This centre might be located in Asia where theclosest relative, P. lateralis, has been found in an old growth Chamaecyparisforest (Brasier et al., 2010). The discovery of a centre of origin might alsoreveal a host with which P. ramorum might have co-evolved, providing amechanism of R gene discovery, a critical tool needed for the managementof sudden oak death. Comparative genomics of related species, such asP. lateralis, P. syringae and P. hibernalis, amongst others, will provide novelinsights into core effectors and genes under purifying selection in the clade,but diverged among clades.

Fig. 5 Impact of sudden oak death in California. Tanoak mortality evidencedby defoliated or wilted canopies on the Bolinas Ridge at Mt. Tamalpais, MarinCounty, CA, USA. Photograph courtesy of Janet Klein (Marin Municipal OpenSpace District).

Fig. 6 Inferred pattern of migration of the four clonal lineages ofPhytophthora ramorum. Modified from Grünwald et al. (2012).



Fig. 7 Silencing machinery in Phytophthora. Phylogenetic placement of dicer-like (DCL) (A) and argonaute (Ago) (B) proteins in the genus Phytophthora. For moredetails, see Fahlgren et al. (2013). Species correspond to: Arabidopsis thaliana, Paramecium tetraurelia, Phytophthora infestans, Phytophthora ramorum,Phytophthora sojae, Tetrahymena thermophila and Toxoplasma gondii.



4. PHYTOPHTHORA SOJAE

Root rot disease of soybean caused by P. sojae was first recognized in NorthAmerica in the 1950s (Hildebrand, 1959; Kaufmann and Gerdemann, 1958).The alternative names P. megasperma var. sojae and P. megasperma f.sp.glycinea were commonly used for this species in the past (Erwin and Ribeiro,1996). Infection of soybean by P. sojae, which is a hemibiotroph, typicallyinitiates below ground and eventually produces spreading cankers thatdestroy root tissues and travel up the stem (Fig. 8). The pathogen thrives inwet conditions and in compacted or heavy clay soils. Motile, water-bornezoospores are released from sporangia and are attracted to soybean rootexudates (Morris and Ward, 1992). Phytophthora sojae is homothallic andcreates abundant, thick-walled sexual oospores that are long lived andprovide a soil-borne inoculum. Phytophthora sojae has a narrow host rangeand its economic damage is limited to soybean. It has been suggested thatP. sojae originated in North America as a pathogen of lupins, as some 26species of the genus Lupinus are susceptible to infection (Erwin and Ribeiro,1996). In laboratory tests, P. sojae can also be made to infect limabean (Phaseolus lunatus), string bean (Phaseolus vulgaris) and cranesbill(Geranium carolinianum) (Erwin and Ribeiro, 1996; Hildebrand, 1959).Phytophthora sojae is one of the most damaging disease problems confront-ing soybean growers (Wrather and Koenning, 2006). The management ofP. sojae in soybean has primarily relied on breeding for resistance.

Research on P. sojae has focused on the mechanisms of pathogen viru-lence, host resistance and the molecular basis of recognition betweenP. sojae and soybean (Dorrance and Grünwald, 2009; Gijzen and Qutob,2009; Tyler, 2007). Phytophthora sojae, together with P. ramorum, was thefirst oomycete to have its genome sequenced (Tyler et al., 2006). Genomicinformation, including gene expression data and multiple genomesequences, have driven rapid progress (Qutob et al., 2000; Torto-Alaliboet al., 2007; Wang et al., 2011). The genome of P. sojae, and later otheroomycetes (Haas et al., 2009), was found to be partitioned into stableregions rich in housekeeping genes displaying extensive synteny with otheroomycete genomes, interspersed with dynamic, transposon-rich regions thatcontained rapidly evolving genes implicated in virulence (Jiang & Tyler, 2012;Tyler et al., 2006) (Fig. 9). Multiple large, rapidly diversifying families ofgenes with functions in virulence were discovered (Jiang and Tyler, 2012;Tyler et al., 2006), including hydrolases, hydrolase inhibitor proteins,

toxin-like proteins, such as the NLP family (Qutob et al., 2006), and twohuge, diverse classes of effector proteins (RXLR and CRN effectors) (Haaset al., 2009; Jiang et al., 2008; Tyler et al., 2006) that can cross into thecytoplasm of host plant cells (Dou et al., 2008; Kale et al., 2010) (Fig. 9). All11 avirulence genes cloned from P. sojae proved to encode RXLR effectorsdetected by host R proteins (Jiang and Tyler, 2012) (Fig. 9). Genetic inherit-ance studies in P. sojae using molecular markers led to discoveries of high-frequency gene conversion (also referred to as loss of heterozygosity)(Chamnanpunt et al., 2001) and epigenetic silencing (Qutob et al., 2013) asimportant mechanisms underlying pathogen variation.

Many areas of future research into P. sojae will be shared with those ofother oomycete and fungal pathogens. One area will be to define in detailhow apoplastic and host cell-entering effectors of P. sojae manipulatesoybean physiology to enable infection, including the soybean moleculestargeted by the effectors (Fig. 9) and the mechanisms by which RXLR andCRN effectors gain entry (Fig. 9). The identification of the P. sojae effectorsmost important for infection (e.g. using new tools for genetic manipulation,such as tailored nucleases) should lead to new targets for disease control.The cell biology of P. sojae infection (Enkerli et al., 1997) must be defined inmuch more detail, incorporating the spatial distributions of pathogen andhost transcripts, proteins and metabolites. Understanding fully the role ofepigenetic mechanisms in the generation of variation in pathogen popula-tions will also be important for the design of effective strategies for diseasecontrol. Sequencing the genomes and transcriptomes of numerous isolatesof P. sojae and its nearest sister species will shed light on the geneticadaptability of the pathogen. In practical terms, a large translationalresearch effort will be required to convert the rapidly accumulating knowl-edge about the basic biology and pathology of P. sojae and other oomycetesinto effective disease control solutions.

Fig. 8 Phytophthora sojae. (A) Diseased soybean plants in the field, infectedwith P. sojae. Plant height is 20–30 cm. (B) Susceptible (left) and resistant(right) soybean plants inoculated in the stem with P. sojae, 7 days afterinfection, illustrating R-gene-mediated resistance. Pots are 10 cm in diameter.(C) Germinating oospore of P. sojae growing on water agar. Oospore is35 μm in diameter. (D) Germinating P. sojae cysts growing on water agar.Cysts are 15 μm in diameter. (E) Etiolated soybean hypocotyls inoculated witha 10-μL water droplet containing 103 zoospores from a virulent (top) andavirulent (bottom) strain of P. sojae, 48 h after infection, illustratingstrain-specific variation in avirulence effectors and the hypersensitiveresponse. Soybean hypocotyls are 5 mm in diameter.

Fig. 9 Large diverse families of virulence proteins encoded by thePhytophthora sojae genome. (A) The Phytophthora sojae genome containsclusters of conserved housekeeping genes (brown) that have conserved ordersamong Phytophthora species, separated by dynamic transposon-rich regionsthat contain genes (red) encoding virulence proteins, many of which aresecreted. (B) Secreted virulence proteins (effectors) may act in the apoplast,or be transported inside the cell. Cell-entering effectors may have targets inthe nucleus or cytoplasm, and may be detected by resistance proteins (Rps;resistance against P. sojae).



5. PHYTOPHTHORA CAPSICI

Phytophthora capsici is a highly destructive invasive pathogen that attackssolanaceous (pepper, tomato), legume (lima and snap beans) and mostcucurbit hosts (Hausbeck and Lamour, 2004; Leonian, 1922). Disease isfavoured by warm (25–28 °C) and wet conditions, and the asexual epidemi-ology is often explosive (Granke et al., 2009). Initial infection is biotrophic,followed by transitions within 24–48 h to necrotrophy and the production ofdeciduous sporangia on the surface of infected tissues (Fig. 10). The impor-tance of the sexual stage differs by region. In Peru and Argentina and acrossmuch of China, long-lived and widely dispersed clonal lineages dominate(Gobena et al., 2012; Hu et al., 2013; Hurtado-Gonzales et al., 2008; Sunet al., 2008). This is in contrast with the USA, South Africa and the northernprovinces of China, where populations have high levels of genotypic diversityand outcrossing is frequent (Dunn et al., 2010; Gobena et al., 2012; Meitzet al., 2010). Once introduced to a field site, P. capsici is difficult to controland often impossible to eradicate. Phytophthora capsici grows rapidly andsporulates heavily on simple media, and isolates from sexual field popula-tions are often fecund (Gobena et al., 2012; Lamour and Hausbeck, 2000).Phytophthora capsici is one of the most genetically diverse eukaryotic organ-isms yet described, and there is significant genetic variation in the form ofsingle nucleotide polymorphisms within individual genomes and acrossworld populations (Lamour et al., 2012).

Current research includes the investigation of resistance (host andnonhost) in commercial vegetable and experimental plants, the discoveryand characterization of genes and proteins driving pathogenicity and viru-lence, and studies to measure the evolution of natural and laboratory popu-lations. Under controlled conditions, P. capsici infects at least 26 plantfamilies (Granke et al., 2012). Natural resistance to P. capsici in pepper andcucurbits appears to be rare (Mallard et al., 2013) but, in tomato, it may beextensive (Quesada-Ocampo and Hausbeck, 2010). Recent molecular studiesof the CRN class of effectors have indicated that they are often localized tothe host nucleus and play an important role in the infection process (Chenet al., 2013; Stam et al., 2013a, 2013b). Transcriptome studies using RNAseqand microarrays have indicated dramatic changes from pre-infective sporesthrough the early biotrophic and later necrotrophic stages of infection (Chenet al., 2013; Jupe et al., 2013). Studies of individual effectors have suggestedthat some manipulate the host to allow infection, whereas others triggerplant cell death (Chen et al., 2013; Feng and Li, 2013; Feng et al., 2010; Sunet al., 2009).

A high-quality reference genome and a high-density single nucleotidepolymorphism-based genetic linkage map have been completed recently(Lamour et al., 2012). These important resources illuminated an importantsource of asexual genetic variation, known as loss of heterozygosity (Lamouret al., 2012). Loss of heterozygosity occurs when variable length tracts(300 bp to >1 Mbp) of the diploid genome switch to one of the two possiblehaplotypes. Loss of heterozygosity has been described in laboratory-produced sexual progeny, field isolates maintained on agar medium and fieldisolates genotyped directly from naturally infected tissue (Gobena et al.,2010; Hu et al., 2013; Hulvey et al., 2010). Loss of heterozygosity is associ-ated with spontaneous switches from the A2 to the A1 mating type, loss ofpathogenicity and reduced virulence (Hu et al., 2013; Lamour et al., 2012).

The diversity and plasticity of P. capsici present challenges and uniqueopportunities for research (Fig. 10). Future research questions include thefollowing. What is the significance of a highly diverse effector arsenal? Arethese effectors important for host-specific interactions and the broad hostrange? How important is loss of heterozygosity in laboratory and fieldpopulations? The genomic plasticity of P. capsici and the ease of laboratorymanipulation provide a unique opportunity to measure genome stability andadaptive evolution at a fine scale, and may provide useful insights into thisand other oomycete pathogens (Lamour and Hu, 2013).

Fig. 10 Heavy sporulation and spontaneous morphological variation in thevegetable pathogen Phytophthora capsici. (A) Naturally infected tomato fruitwith sporangium production on the surface of the fruit. (B) A singlezoospore-derived field isolate of P. capsici sectoring on V8 agar mediumfollowing long-term storage.



6. PLASMOPARA VITICOLA

The obligate biotrophic oomycete Pl. viticola, the causal agent of grapedowny mildew, is native to North America and was inadvertently introducedinto Europe at the end of the 19th century (Millardet, 1881; Viennot-Bourgin,1949), causing severe damage to Vitis vinifera, which had evolved in theabsence of this pathogen (Galet, 1977; Gessler et al., 2011). Plasmoparaviticola belongs to the family Peronosporaceae; its life cycle includes anasexual multiplication phase occurring during the plant vegetative periodand a sexual phase that ensures pathogen overwinter survival (Wong et al.,2001). The pathogen overwinters as oospores in dead leaf lesions or asmycelium in infected twigs. In spring, and in particular during rainy periods,oospores germinate to produce sporangia, which are transported by wind orwater to the wet leaves near the ground, which they infect through stomataon the lower surface. The mycelium then spreads into the intercellular spacesof the leaf from which sporangiophores arise and emerge through the stoma,ready to start new infection cycles (Gobbin et al., 2005). Downy mildewaffects leaves, fruits and shoots, with young tissues being particularly sus-ceptible to infection (Fig. 11) (Kennelly et al., 2007).A disease cycle may takefrom 5 to 18 days, depending on the temperature, humidity and varietalsusceptibility (Agrios, 2005; Gessler et al., 2011).

Downy mildew is still most destructive in Europe and in the eastern halfof the USA, where it may cause severe epidemics year after year (Agrios,2005; Madden et al., 1995). When the weather is favourable and no protec-tion against the disease is provided, downy mildew can easily destroy up to75% of production in a single season (Madden et al., 2000; Rossi and Caffi,2012). Occasionally, Pl. viticola can be destructive in other humid parts of theworld in which V. vinifera is cultivated.

In the last 50 years, research on grapevine downy mildew has focused onthe pathogen life cycle and epidemiology (reviewed in Gessler et al., 2011),and on the genetic identification of host resistance loci for the establishmentof molecular markers (revised in Töpfer et al., 2011). In the last decade,studies on Pl. viticola have highlighted its enormous potential in the devel-opment of fungicide resistance (Blum et al., 2010; Chen et al., 2007) and inbreaking down plant resistance of interspecific hybrids, such as ‘Bianca’(Casagrande et al., 2011; Peressotti et al., 2010) and ‘Regent’ (Delmotteet al., 2013). Population genetic studies have been carried out (Fontaineet al., 2013 and references therein) to assess pathogen dynamics and diver-sity in Europe. Moreover, it has been proposed that grapevine downy mildewis not caused by a single species, but instead by a complex of cryptic speciesthat have diverged on Vitaceae (Rouxel et al., 2013). Trade-offs between thesize and number of sporangia produced have been reported, leading toecological advantages for this pathogen (Delmotte et al., 2013). For thesereasons, the Vitis–Pl. viticola pathosystem was elected as a prime candidatefor the study of host specialization of biotrophic plant pathogens (Rouxelet al., 2013) and pathogen adaptation to partial host resistance (Delmotteet al., 2013).

Control methods against Pl. viticola are essentially based on the use ofchemical fungicides and the application of disease models that serve asdecision support systems (Lalancette et al., 1987; Rossi et al., 2009, 2013;Vercesi et al., 2010). As a result of the growing public concern on the use ofchemical pesticides, and the need to adhere to the European Directive2009/128/EC encompassing a framework ‘to achieve a sustainable use ofpesticides’ by promoting Integrated Pest Management (IPM), the search foralternative methods for the control of Pl. viticola on grapevine appears to beurgent. Several alternative approaches have been proposed in the last20 years, but none has been transferred to practical use (Gessler et al.,2011). Moreover, the lack of precise characterization of Pl. viticola isolates isdramatically limiting the reliable control of the pathogen. Although molecu-lar studies have previously confirmed a high diversity in the pathogen popu-lation, there is a surprising lack of phenotypic characterization of pathotypestrains or races which could be used to study the mechanisms of interactionwith host genotypes with different levels of resistance (Gómez-Zeledónet al., 2013). In conclusion, interdisciplinary studies and consistent resourcesshould be invested for the study of the Pl. viticola–V. vinifera pathosystem inorder to find new, effective alternatives for the IPM of this highly adaptiveand destructive pathogen.

A

B

Fig. 11 Downy mildew symptoms with well-evident sporangiophores on thelower side of a grape leaf (A) and a young cluster (B).



7. PHYTOPHTHORA CINNAMOMI

Some call it the ‘biological bulldozer’ for its capacity to destroy naturalplant communities across the globe, and disease caused by P. cinnamomihas broad and economically important impacts in forestry and horticulture,and in the nursery industry. Like other Phytophthora spp., P. cinnamomihas a number of strategies for survival, propagation and dissemination. Themotile zoospore is recognized as the main infective propagule followingencystment and attachment to roots and stems (Fig. 12). Recent work hassuggested that, in addition to chlamydospores, P. cinnamomi is also asso-ciated with lignituber formation which enables survival under harsh con-ditions (Jung et al., 2013). Both A1 and A2 mating types are pathogenic,but wide differences in the distribution and frequency of occurrencesuggest that the A2 mating type is more invasive and is generally recog-nized as being the more aggressive of the two mating types. Where intro-duced, this pathogen has had enormous impacts on natural systems,including those of Australia, southern Europe and the USA. In Australia, forexample, it has been estimated that >3000 largely endemic plant speciesfrom numerous plant families are under threat, and a new National ThreatAbatement Plan has been urgently implemented (Australian GovernmentDepartment of Environment, 2014) (Fig. 13). The control of disease, espe-cially across the large areas of native vegetation affected, is still a greatproblem, but some success has been achieved by the use of phosphite inboth natural systems and in agriculture (Akinsanmi and Drenth, 2013;Crane and Shearer, 2014), by the use of calcium amendments to soil(Serrano et al., 2013) and by containment and eradication of spot infec-tions (Dunstan et al., 2010). Climate change is predicted to have a signifi-cant influence on the intensity and distribution of disease (Thompsonet al., 2014).

Phytophthora cinnamomi is a challenging organism to work with.Sequencing of its genome has recently been completed (JGI; http://genome.jgi-psf.org/) and has opened up a variety of opportunities to inves-tigate the critical features that enable this pathogen to be so wide-rangingin its hosts. A real change in emphasis in research on P. cinnamomi hasoccurred in recent times, with an increasing number of groups usinggenomic, transcriptomic and proteomic approaches to understand thepathogen and/or its interaction with the host (for example, Reeksting et al.,2014). Experimental plants, including Arabidopsis, Zea mays and Eucalyptus,for which comprehensive genomic information is available, are increasinglybeing used as host–pathogen platforms (for example, Allardyce et al., 2013;Dempsey et al., 2012; Rookes et al., 2008). Fundamental studies onP. cinnamomi plant cell wall-degrading enzymes and the genes that encodethem are being undertaken (Hee et al., 2013; Adrienne Hardham, AustralianNational University, Canberra, ACT, Australia, personal communication), aswell as examination, at the molecular level, of defence pathways and theircontrol (Eshraghi et al., 2014; Gunning et al., 2013).

High-throughput, genome sequencing is emerging as an exciting way toexamine the pathogen, its hosts and the soil environment, and is now beingused to examine pathogen ecology and diversity within soils, and for theanalysis of the response of host plants (Treena Burgess, Murdoch University,Perth, WA, Australia, personal communication). Much of our progressin understanding host–pathogen interactions will come from suchapproaches. We still lack knowledge on why plants are resistant to thispathogen and what is the basis for induced resistance, for example, fol-lowing phosphite treatment. The search for host resistance to P. cinnamomiis an active area in which signalling pathways and their control are beingelucidated. Mapping the disease over the large invaded areas is still notstraightforward, although advances in remote sensing, high-resolutiondigital photography, hyperspectral imaging (David Guest, Sydney University,Sydney, NSW, Australia, personal communication) and ‘drone’ technologywill probably see our ability in this area being greatly enhanced in the nearfuture. The era of nanotechnology offers new opportunities for the deliveryof molecules that can influence disease outcome, yet this area has not beenexplored to date, although preliminary research with various nanoparticlesystems (Hussain et al., 2013; Nadiminti et al., 2013) has indicated thatthese may be useful in delivering molecules, including pathogen effectors,DNA and miRNA, which may modify host processes and their response topathogen infection.

Future research will focus on the following questions. (i) What are thevirulence factors that enable P. cinnamomi to infect and colonize suscep-tible species and therefore should be targeted for control? (ii) What con-stitutes host resistance and how can it be manipulated? Can we look tonanotechnology for some answers? (iii) Is phosphite the only chemical thatwe can use to control P. cinnamomi, and how does phosphite alter thehost response?

Fig. 12 Cryo-scanning electron micrograph of a Phytophthora cinnamomicyst between two epidermal cells on a root of tobacco. Note the adhesivematerial that surrounds the cyst that has been expelled by zoosporeperipheral vesicles. Photograph courtesy of Adrienne Hardham, AustralianNational University.

Fig. 13 (A) Individual plants of Xanthorrheoa australis (austral grass tree), ahighly suscpetible native Australian species, infected by Phytophthoracinnamomi within a dry sclerophyll eucalypt forest at Anglesea, Victoria,Australia. Note the dead and dying plants that have brown, collapsed leavescompared with the healthy green and erect leaves of plants which are yet tobe killed. These individual plants range in age from approximately 20 years(the smallest in the centre) to around 70 years (green individual on the rightof the image). (B) Advancing disease front caused by invasion byP. cinnamomi in Xanthorrhoea australis-dominated understorey in eucalyptusopen forest at Wilsons Promontory, Victoria, Australia. The disease has movedfrom the foregound of the picture, where all susceptible vegetation includingX. australis has been killed, and its progress can be seen as a line of deadand dying X. australis (brown collapsed plants) at the disease margin. Healthygreen plants behind them will soon be killed. Loss of the major understoreycomponents, as in the forground, results in complete structural change andloss of all susceptible species.



http://genome.jgi-psf.org/

http://genome.jgi-psf.org/

8. PHYTOPHTHORA PARASITICA

Phytophthora parasitica (= P. nicotianae) is a worldwide distributed patho-gen (Erwin and Ribeiro, 1996). Primarily known to cause tobacco black shankand citrus root rot and gummosis (Fig. 14), it is also responsible for severefoliar and fruit diseases, as well as root and crown rots on herbaceous andperennial plant species in more than 250 genera, including solanaceouscrops (Fig. 15), and horticultural and fruit trees (Cline et al., 2008).Phytophthora parasitica produces both asexual zoospores and thick-walledsexual oospores. Oospores constitute a potential source of genetic variationand, with resting chlamydospores, contribute to survival in unfavourableconditions in soil or within infected plant tissues.

Contrasting with the broad host range observed at the species level, mostindividual P. parasitica isolates display host preference (Erwin and Ribeiro,1996). Frequent cases of differential virulence on a range of hosts have beenrevealed (Colas et al., 1998; Matheron and Matejka, 1990), pointing out the

need to decipher the genetic structure of P. parasitica on a global scale. Inagreement with pathogenicity tests, recent single nucleotide polymorphismanalyses conducted with mitochondrial and nuclear genes have revealed aspecific association between the host of origin and genetic grouping whichwas particularly evident for tobacco and citrus isolates (Mammella et al.,2011, 2013). In contrast, no clear genetic structure was revealed for isolatesfrom other hosts, especially potted ornamentals in nurseries. A significantgeographical structuring was revealed for tobacco, but not for citrus, isolates(Bonnet et al., 1994; Colas et al., 2001; Mammella et al., 2013). Furtherstudies relying on whole-genome sequencing programmes (see below) arenecessary to determine whether these molecular groups represent evidenceof physiological races, pathotypes or even subspecies within P. parasitica.

As some isolates may also infect many hosts, including Arabidopsisthaliana (Attard et al., 2008, 2010), P. parasitica has emerged as an idealpathogen to develop specific studies with the aim to advance our knowledgeon the mechanisms underlying general pathogenicity and those governinghost specificity. Furthermore, P. parasitica is phylogenetically related to

Fig. 14 Impact of Phytophthora parasiticainfection on citrus plants. (A, B) Five-year-oldcitrus plants not infected and infected,respectively, with Phytophthora parasitica. (C,D) Symptoms of P. parasitica on stems: (C) notinfected; (D) infected plant displayinggummosis symptoms. (E, F) Leaves and fruits ofinfected (left) and healthy (right) plants. (G, H)Scanning electron microscope images of citrusfine roots infected with P. parasitica. Yellowarrows show encysted zoospores and germtube of P. parasitica. Bar represents 20 μm.(A–F) Photographs courtesy of R. J. D. Dalio.(G, H) Photographs courtesy of M. E.Escanferla.



P. infestans in Phytophthora clade 1, and overlaps its host range, whichincludes potato (Taylor et al., 2008). Comparative analyses on these twospecies varying in genome size (83 and 240 Mb for P. parasitica andP. infestans, respectively) will facilitate the understanding of the evolutionbehind pathogenicity and host range among Phytophthora spp. Through thesequencing of the genome of isolates of diverse host range and geographicalorigins, the international ‘Phytophthora parasitica genome initiative’ projectwill enable the characterization of genes that determine host range. In-depthgenomic and transcriptomic analyses of 14 sequenced genomes are currentlybeing performed. Special efforts are being devoted to characterize the rep-ertoire of effector proteins. As a broad host range pathogen, P. parasiticaprovides a unique opportunity for intra- and interspecific comparative analy-ses, looking for the presence of various effector families, their organization,their role in plant recognition and infection, and their evolution amongstrains and species that display broad or restricted host ranges. The identi-fication of conserved effector groups, as well as of other pathogenicitygenes, will allow the evaluation of the evolutionary pressures of exposure todifferent host defence responses to the diversification of effectors and theirrole in adaptation to host plants.

Phytophthora parasitica has not been as extensively studied as its eco-nomic importance should warrant. However, it is likely to gain importance inthe foreseeable future for the following reasons. First, it is prominent innurseries of potted ornamentals and fruit tree species, the trade of whichseems to represent one of the most efficient dissemination pathways ofPhytophthora (Moralejo et al., 2009; Olson and Benson, 2011). This makesP. parasitica an ideal species to study diffusion pathways of Phytophthoraand other soil-borne pathogens on a global scale. For aesthetic reasons, theornamental industry requires the extensive use of anti-oomycete chemicals(Olson et al., 2013). The global nursery trade thus increases the risk of therapid spread of resistant P. parasitica strains to new areas following theinappropriate use of fungicides, and constitutes a growing threat to localagriculture and natural ecosystems (Brasier, 2008). In addition, P. parasiticawill probably benefit from the warming climate. Its host range generallyincludes those of other species of prime economic importance (P. infestans,P. capsici, P. citrophthora), but generally requires warmer conditions thanthese potential competitors (Erwin and Ribeiro, 1996). Consequently, theforeseen global warming is likely to provide a catalyst for the geographicalexpansion of this species, as has already been proposed in Mediterraneanclimates (Andres et al., 2003; Saadoun and Allagui, 2008) and in easternIndia (Guha Roy et al., 2009).

Fig. 15 Severe infection of brinjal fruit with Phytophthora parasitica. Typicalsymptoms are brown, soft, water-soaked patches which rapidly cover thewhole fruit. Brinjal is also known as aubergine or eggplant (Solanummelongena). Photograph courtesy of S. Guha Roy.



9. PYTHIUM ULTIMUM

Pythium resides in the peronosporalean lineage of oomycetes, withPhytophthora and downy mildews (Dick, 2001). One of its most significantmembers is Py. ultimum, which causes damping off and root rot on >300diverse hosts, including corn, soybean, wheat, Douglas fir and ornamentals(Farr and Rossman, 2014). Pythium ultimum is a common inhabitant offields, ponds and streams, and of decomposing vegetation worldwide. Con-tributing to the ubiquity of the species is its ability to grow saprotrophicallyin soil and plant residue, a trait shared by most Pythium spp., but not otherperonosporaleans, which must colonize living hosts. Pythium ultimum is alsohomothallic, producing oospores capable of long-term survival (Martin andLoper, 1999). Mycelia and oospores in soil can thus initiate infections ofseeds or roots, leading to wilting, reduced yield and mortality (Fig. 16A).Disease management is difficult, but focuses on sanitation, fungicides andbiological control, particularly in glasshouses. Quantitative resistance hasbeen reported in several hosts, but has a limited effect (Lucas and Griffiths,2004; Wang and Davis, 1997).

The role of asexual spores depends on the strain. Pythium ultimum is aspecies complex that includes Py. ultimum var. ultimum and var.sporangiiferum, which have indistinguishable internal transcribed spacer(ITS) sequences (Schroeder et al., 2013). Sporangia and zoospores are pro-duced rarely by the former, but abundantly by the latter. Pythium ultimumvar. ultimum forms sporangia-like hyphal swellings which germinate to yieldinfective hyphae (Fig. 16B; Stanghellini and Hancock, 1971). Similar to otheroomycetes, it also produces sexual oospores (Fig. 16C).

Genome sequencing of several Pythium spp., including Py. ultimum var.ultimum and var. sporangiiferum, has provided insight into their biology(Adhikari et al., 2013; Levesque et al., 2010). Annotated in the c. 43-Mbgenomes of two subspecies are 15 290 and 14 086 genes, respectively,which is less than the smallest Phytophthora, but more than downy mildews.Whether this difference in gene number is significant requires more analysis,as the two assemblies vary in quality and only single isolates weresequenced. Large size variation between isolates was reported on the basisof electrophoretic karyotyping (Martin, 1995).

Nevertheless, it is evident from genome analysis that there are manydifferences between Pythium and Phytophthora, including a 25% reductionin Pythium of the fraction of proteins that are secreted. In part, this reflectsthe absence of RXLR effectors, which may not be needed for necrotrophiclifestyles. Pythium also lacks haustoria, which appear to be used bybiotrophic and hemibiotrophic oomycetes to deliver RXLRs to host cells(Whisson et al., 2007).Another likely sign of the necrotrophy of Pythium is itsgreater abundance of lipases and proteases. However, Pythium lackscutinases and pectin esterases, but this is probably because it infects pri-marily nonsuberized tissue, whereas Phytophthora (which encodes theseenzymes) can penetrate plant cuticles. Pythium encodes sufficient enzymesfor the maceration of host cell walls, but cannot degrade some ubiquitouswall components, such as xylans, which suggests that soluble sugars may bea more important carbon source (Zerillo et al., 2013).

Markers derived from Py. ultimum genomes should help reveal whatdistinguishes the subspecies and provide more resolution to populationstudies, which can help to identify the sources of outbreaks. Studies ofPy. ultimum var. ultimum have indicated that populations are not clonal andsome outcrossing may occur (Francis and St. Clair, 1997). A greater evolu-tionary question concerns the organization of the Pythium genus as a whole.Division of the >120 Pythium species over five new genera has been pro-posed on the basis of the sequence analysis of two loci (Uzuhashi et al.,2010). If accepted by the community, Py. ultimum would be renamedGlobisporangium ultimum.

Of much interest is the interaction between Py. ultimum and biocontrolagents, such as Trichoderma, Streptomyces, Pythium oligandrum (amycoparasitic member of the genus) and others (Gracia-Garza et al., 2003;Martin and Loper, 1999). The extent to which these organisms function byaltering rhizosphere microflora or attacking Py. ultimum directly is an openquestion (Naseby et al., 2000; Vallance et al., 2012); Pythium ultimum com-petes poorly with organisms having higher saprotrophic capabilities.

Pythium ultimum is just one of many destructive members of the genus,with Py. aphanidermatum and Py. irregulare also topping lists of important

pathogens (Martin and Loper, 1999). Opportunities for understanding theirbiology, ecology and evolution have been enhanced by genome sequencing.DNA-mediated transformation has been achieved for several species, butfew studies of gene function have been reported (Grenville-Briggs et al.,2013; Weiland, 2003). As core promoter structure appears to be conservedwithin the Peronosporales, vectors and technologies applied to species, suchas Phytophthora, should be transferable to Pythium (Roy et al., 2013).Pythium spp. are easily grown and have the potential to develop into valu-able experimental systems for necrotrophic and saprotrophic oomycete life-styles. Their growth on byproducts of the agro-food industry has alsoattracted interest as sources of polyunsaturated fatty acids for human con-sumption (Stredansky et al., 2000).

Fig. 16 Pythium ultimum var. ultimum. (A) Pre-emergence damping-off inokra, resulting in the death of most plants at the front of the row. At theback, disease was controlled using metalaxyl. (B) Terminal hyphal swellings;bar, 10 μm. (C) Oospore within oogonium; bar, 10 μm. Images adapted fromKida et al. (2006) with permission.



10. ALBUGO CANDIDA

White blister rust is a disease caused in many dicotyledonous plant speciesby obligate biotrophic parasites. For example, A. candida infection ofBrassica juncea (Indian mustard) has resulted in significant crop losses inIndia (Awasthi et al., 2012), Canada (Rimmer et al., 2000) and Australia(Kaur et al., 2008). The white rusts, order Albuginales, are phylogeneticallydistant from the Peronosporales, and probably represent an independentacquisition of biotrophy (Thines and Kamoun, 2010; Thines and Spring,2005). All Albugo species infecting the Brassicaceae were thought to beraces of A. candida, but molecular studies of isolates from various hosts andlocations have led to the description of specialists, for example Albugolaibachii on Arabidopsis thaliana (Thines, 2014; Thines et al., 2009). SpecificA. candida races can grow on diverse plant hosts, including Brassicaceae,Cleomaceae and Capparaceae (Thines, 2014). Albugo spp. provide an inter-esting experimental system for the study of plant immune suppression,disease resistance and host–pathogen co-evolution.

Albugo spp. reproduce asexually via zoosporangia, which release flagel-lated motile zoospores on incubation in water. On the surface of a plant leaf,zoospores settle in stomata, and each extends a germ tube into thesubstomatal chamber (Holub et al., 1994). Coenocytic hyphae then growintercellularly through the plant. Small globose haustoria penetrate intoplant cells (Soylu et al., 2003). When an Albugo infection is mature,zoosporangia rupture the plant epidermis with force and enzymatic diges-tion (Heller and Thines, 2009). This results in characteristic ‘white blister’pustules. Albugo also has a sexual cycle, producing tough oospores that cansurvive difficult environmental conditions (Petrie, 1975). During the systemicinfection of Brassicaceae hosts, the inflorescences become misshapen,forming so-called ‘stagheads’ (Fig. 17A).

Albugo infection has long been associated with ‘green islands’, whereinfected tissue appears to be healthy and senescence is delayed. Infection byAlbugo also greatly enhances susceptibility to co-infections with downymildews (Bains and Jhooty, 1985; Crute et al., 1994). Cooper et al. (2008)investigated the ability of A. laibachii and A. candida to suppress hostimmunity. They showed that A. laibachii can suppress the ‘runaway celldeath’ of Arabidopsis lsd1 mutants after inoculation with avirulentH. arabidopsidis. Furthermore, when pre-infected with virulent A. laibachii,resistant Arabidopsis accessions were no longer resistant to avirulentH. arabidopsidis isolates (Fig. 17B), lettuce downy mildew or powderymildew. Suppression was also observed on B. juncea with A. candida andBrassica downy mildew (Cooper et al., 2008). These results suggest thatAlbugo is effective at broad suppression of plant immunity, includingeffector-triggered immunity.

The first step in understanding how Albugo spp. impose such susceptibil-ity is to examine their genomes. Links et al. (2011) and Kemen et al. (2011)sequenced A. candida and A. laibachii genomes, respectively. The genomesare around 40 Mb and compact; about 50% of the assemblies consist ofcoding sequences (see Fig. 18). Both genomes show adaptations to obligatebiotrophy; they are missing sulfite oxidases, nitrate and nitrite reductasesand, in the case of A. laibachii, the whole molybdopterin biosynthesispathway. The A. candida secretome consists of 929 proteins (withouttransmembrane domains), compared with 672 in A. laibachii, perhapsreflecting its wider host range.Within the secretomes, there is no enrichmentof putative RXLR effectors. Kemen et al. (2011) discovered the CHXC(cysteine, histidine, any amino acid, cysteine) motif at the N-terminus of aclass of candidate effectors. The CHXC-containing N-terminus is sufficient totranslocate the C-terminus of P. infestans AVR3a (an RXLR effector) into hostcells (Kemen et al., 2011).

Several A. candida races can infect some, but not all, A. thaliana acces-sions and, from crosses between resistant and susceptible accessions, an Rgene against four A. candida races, WRR4 [encoding a toll interleukin 1receptor-nucleotide-binding-leucine-rich repeat (TIR-NB-LRR) R protein],was identified (Borhan et al., 2008). WRR4 can also provide resistance toA. candida when transformed into susceptible cultivars of B. napus andB. juncea (Borhan et al., 2010). In A. thaliana, RAC1 (also encoding a TIR-NB-LRR R protein) confers resistance to A. laibachii (Borhan et al., 2004).The inheritance of avirulence of a B. juncea isolate (Ac2V) was studiedthrough a cross between two A. candida isolates; this work predicted a

single avirulence gene for the incompatibility between Ac2V and B. rapa(Adhikari et al., 2003).

There are open questions about Albugo from both fundamental andtranslational perspectives. Thines (2014) speculated that the broad hostrange of the A. candida meta-population is maintained through frequentgenetic exchange where the host range of individual isolates overlap. Com-paring the genomes of multiple isolates from different hosts would test thishypothesis and build up a clear picture of population variation. This wouldalso aid the discovery of new effector candidates through the identificationof secreted proteins under strong selective pressure. A more extensive analy-sis of Albugo effectors should be made. The presence of the CHXC effectorsinside host cells needs to be confirmed and the translocation mechanismelucidated. It is unclear which Albugo effector proteins are recognized by thefew known R proteins. Arabidopsis thaliana cannot be colonized by mostA. candida isolates. The molecular basis for this resistance could be exploitedto introduce durable resistance to Brassica crops.

Lastly, and perhaps most interestingly, is the question: how does theremarkable defence suppression by Albugo work? We need to define theextent of this suppression. What other pests or pathogens can grow onplants infected with Albugo? What changes occur in the microbiome ofAlbugo-infected leaves in the field? Recent data have suggested that Albugocould be widespread as an asymptomatic endophyte (Ploch and Thines,2011). The implications of these infections as a reservoir for (i) Albugo and(ii) further Albugo suppression-enabled infections by other species remain tobe discovered.

Fig. 17 Disease symptoms of Albugo infections. (A) Disease resulting fromthe infection of Brassica juncea with an unknown Albugo species. Themisshapen inflorescence phenotype is known as a ‘staghead’. (B) An exampleof immunity suppression by Albugo laibachii: A. thaliana Col-0 is resistant toHyaloperonospora arabidopsidis Emoy2 via RPP1 but, when pre-infected withA. laibachii, can support the growth of both pathogens.



CONCLUSION

Although the study of oomycete plant pathogens has always been an impor-tant topic in plant pathology, it has recently taken an even more central rolewith the advent of genomics and the discovery of large effector repertoires inoomycete genomes.This article provides a benchmark for future trends. Manytopics remain to be investigated in more depth. For example, the large numberof pathogenic species and the wide diversity of host species and host rangesshould provide a rich basis for the investigation of the genetic and physio-logical mechanisms of host adaptation and specialization. It will also beinteresting to track how the Top 10 list will develop in the coming years. Manypathogenic oomycetes among the 33 listed (Table 2) have evolved uniqueadaptations in their parasitic lifestyle that will undoubtedly reveal fascinatingprocesses and mechanisms. Thus, future research efforts should take intoaccount a diverse spectrum of taxa beyond the widely studied species.

ACKNOWLEDGEMENTS

The authors would like to thank Dr Diane Hird for assistance with severalaspects of the project.

Sophien Kamoun, Oliver Furzer and Jonathan D. G. Jones receivedfunding from the European Research Council (ERC), the UK Biotechnologyand Biological Sciences Research Council (BBSRC) and the Gatsby Chari-table Foundation. Ronaldo Dalio thanks the National Council for Scientificand Technological Development (CNPq/CsF Brazil—313139/2013-0) forfinancial support. Michelina Ruocco receives support from ConoscenzeIntegrate per Sostenibilità ed Innovazione del Made in ItalyAgroalimentare(CISIA–MIUR). Leonardo Schena was supported by grant FIRB 2010—RBFR10PZ4N from the Italian Ministry of Education, University andResearch (MIUR).Andreia Figueiredo receives support from the PortugueseFoundation for Science and Technology (Grant n° SFRH/BPD/63641/2009).Xiao-Ren Chen was financed by the National Natural Science Foundation ofChina (Grant no. 31101395) and Jiangsu Province Basic Research Program(Natural Science Foundation) of China (Grant no. BK2011443). Howard S.Judelson and Brett M. Tyler were supported by grants 2011-68004-30154and 2011-68004-30104, respectively, from the Agriculture and FoodResearch Institute of the National Institute of Food andAgriculture of the US

Department of Agriculture. Mark Gijzen was supported by the Agricultureand Agri-Food Canada GRDI program. Niklaus J. Grünwald was supportedby grant 2011-68004-30154 from the US Department of AgricultureNational Institute of Food and Agriculture, the National Research InitiativeCompetitive Grants Program grant 2008-35600-18780, the US Departmentof Agriculture Agricultural Research Service CRIS 5358-22000-039-00D, theNorthwest Center for Nursery Crop Research, the US Forest Service, the USDepartment of Agriculture Agricultural Research Service FloricultureNursery Initiative and Oregon Department of Agriculture/Oregon Associa-tion of Nurseries. Daniel F. A. Tomé is funded by the UK Biotechnology andBiological Sciences Research Council grant BB/G015066/1. John McDowellis supported by the US Department of Agriculture–Agriculture and FoodResearch Initiative (2009-03008 and 2011-68004), the National ScienceFoundation (ABI-1146819) and the Virginia Tech Institute for Critical Tech-nology and Applied Sciences. Fouad Daayf received funding from acronymsare: The Natural Sciences and Engineering Research Council of Canada(NSERC), Manitoba Agri-Food Research and Development Initiative (MB-ARDI), McCain Foods, Keystone Potato Producers Association (KPPA) andPeak of the Market. Harold J. G. Meijer is funded by The Dutch TechnologyFoundation STW-NWO (VIDI grant 10281). Benjamin Petre is supported byan INRA Contrat Jeune Scientifique and has received the support of theEuropean Union, in the framework of the Marie-Curie FP7 COFUND PeopleProgramme, through the award of an AgreenSkills fellowship (under grantagreement n°267196). Francine Govers receives support from the Food forThought Program, Wageningen University Fund.

AUTHOR CONTRIBUTIONS

All authors voted and contributed to the writing of the 10 sections. SKoversaw the voting and writing. Other authors are listed in reverse orderbased on the species ranking. The species coordinators are listed last in theirsection and are preceded by other contributors listed in alphabetical order.The species coordinators are: Albugo candida (OF and JDGJ), Pythiumultimum (HSJ), Phytophthora parasitica (FP), Phytophthora cinnamomi (DC),Plasmopara viticola (MR and AF), Phytophthora capsici (KL), Phytophthorasojae (MG and BMT), Phytophthora ramorum (NJG), Hyaloperonosporaarabidopsidis (GvdA and JMcD) and Phytophthora infestans (PRJB and FG).

Fig. 18 Albugo spp. have compact genomes. Synteny between Albugo laibachii, Pythium ultimum, Hyaloperonospora arabidopsidis and Phytophthora infestans. Theregion shown is an example of the relatively dense clustering of genes in Albugo species. With increasing genome size, the distance between both genes increasesand re-organizations occur (red, synteny without inversion; blue, inverted regions). Reproduced from Kemen et al. (2011).



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The Top 10 oomycete pathogens in molecular plant pathology